Animals without oxygen and their implications for the evolution of life

It’s been a slow few weeks around here at Culturing Science. It’s due to a little bit of writer’s block, but mainly it’s just the beautiful weather keeping me outdoors and away from the computer. Hopefully you’ve been outside so much that you haven’t noticed.

But today my dream article was published: microorganisms, extreme environments, evolution, and daydreaming all rolled into one. I couldn’t resist but write it up in an excitement-driven fury. (The 90 degree weather in Philadelphia is also a little too hot for my taste.)

Are you sitting down? Today scientists from the Polytechnic University of Marche (Ancona, Italy) and the Natural History Museum of Denmark published their discovery of the first multi-cellular animals found to survive without oxygen. You’ve probably heard of Archaea or Bacteria species which are able to survive in extreme temperatures, acid, or sulfur-rich environments – places we wouldn’t dream of living. And the world at large is fascinated by them for this reason.

For this study, the scientists collected sediment core samples from the L’Atalante basin in the Mediterranean. This basin is completely anoxic (oxygen-free), with a salty layer of brine above forming a physical barrier preventing any oxygen from reaching the area. In the sediment, they found traces of animals from three phyla: Nematoda, Arthropoda and Loricifera.

However, as all the animals were dead upon analysis, they had to confirm that these animals were in fact living in the sediment, and hadn’t simply settled there in a “rain of cadavers” (What poetry!) from oxygenated areas of the sea. They treated the specimens with a stain that binds to proteins – presumably dead animals would have fewer proteins due to decomposition. In the figure to the right, we see little protein in the Arthropoda (a) and Nematoda (b) images. However, the Loricifera (c) specimen is bright pink, indicating protein. The arthropod and nematode species are thus probably dead bodies or shed exoskeletons – but the Loriciferan (unstained in f) shows promise of actual life in the oxygen-free sediment.

After staining more specimens, the researchers also noticed eggs (d and e) within the bodies of the Loriciferans. This is a novel find because it suggests that these animals do not just spend part of their lifecycle in the anoxic sediment, but live without oxygen for their entire lives, including reproduction. They additionally found exoskeletons from young Loriciferans (g) suggesting that these eggs grow up in the sediment as well. While it would still be a new discovery to science if we found animals that live part of their lives in anoxic conditions, the fact that they spend their entire lifecycles down there raises many more questions and expands our definition of life on this planet.

To further confirm that these bugs are living in the sediment, the team gathered fresh sediment samples and added radioactive protein to see if the Loriciferans would eat it. They traced this radioactivity and found that the animals had incorporated the radioactive substrate into their bodies providing final evidence that these guys are in fact living without oxygen.

So what’s the big deal about a multicellular organism living without oxygen? Why am I nearly peeing myself over this? We already know about single-celled organisms can live in extreme conditions. Why is this so exciting?

It makes sense that single-celled organisms would be more likely to survive in weird places because they can adapt to environments more easily. They only have one cell to take care of, so if that one cell is viable, they’re fine. In addition, single-celled organisms are more likely to transfer genes between one another, allowing adaptations to spread more quickly. But it was assumed that we don’t find multicellular life in extreme conditions because more complex life simply could not exist there.

But now we have found a multicellular animal that can survive without oxygen. And the million dollar question: how did it evolve that way? In their findings, Danovaro et al. mention that the Loriciferans don’t appear to have mitochondria, which are found in oxygen-consuming animals, but rather hydrogenosomes, which are found in some single-celled organisms living in extreme environments. This presents the possibility of endosymbiosis – or the incorporation of one organism into the other. Endosymbiotic theory is widely accepted to explain mitochondria and chloroplasts in cells; perhaps this occurred another time for the hydrogenosomes of the Loriciferans. This suggests that maybe this is not as rare of an event as we thought – who knows what other organelles have evolved this way, including ones we haven’t identified yet.

This finding has implications for how we think about the evolution of life on earth. We humans are obsessed with ourselves; since we breathe oxygen, it’s often assumed that life on earth evolved once oxygen was around. The discovery of these non-oxygen-breathing animals provides evidence that multicellular life could have risen prior to oxygen, supporting evidence that early life evolved in highly acidic conditions. (For more on this, see Marek Mantel and William Martin’s commentary on this paper.)

But let’s get down to the real business: let’s talk about space and aliens. Thus far, we have been primarily searching for alien life based on oxygen because we have lacked proof that complex life can exist that isn’t oxygen based. The only life we know – us – is oxygen based, providing no other models of life besides planets with oxygen. The prior knowledge of only single-celled organisms living in non-oxygen based environments suggested that intelligent life cannot exist in those systems. And while I wouldn’t consider Loriciferans (also known as “brush-heads”) intelligent, they do suggest that non-oxygen substrates can support higher life. So when looking for aliens, let’s stop being so anthropocentric. Life can survive without oxygen.

10 Responses

endosymbiosis seems an unlikely explanation. Most of the single-celled Eukaryotes with hydrogenosomes appear to have evolved them directly from mitochondria. In addition, this appears to have happened independently in most of the various lineages involved. Further, there are several animals with facultatively anaerobic mitochondria, which also appear to have evolved them independently.

When thinking about this, I was simply following Occam’s razor – that the simplest answer is the best. Since hydrogenosomes are found in many different lineages, I thought it made more sense for them to have evolved once and been incorporated endosymbiotically multiple times than to have evolved similarly many times throughout history.

But perhaps you are more of an expert. Is hydrogenosome a blanket term to describe many types of anaerobic mitochondria, or does it refer to a specific form of organelle?

AFAIK a hydrogenosome is an organelle that produces hydrogen, presumably as a by product of its energy production. The evidence is pretty strong they evolved several times, at least semi-independently in several lineages, based on the papers mentioned above (linked in my post, the top one on my blog at the moment). Especially see:

4 Organelles in Blastocystis that Blur the Distinction between Mitochondria and Hydrogenosomes Open Access

6 Degenerate mitochondria Open Access

and

8 Mitochondria as we don’t know them

(The actual links are in my post, I didn’t want to try pasting them here since there’s no preview function. All are peer-reviewed papers although #8 links to a non-official version, since the official one’s behind a paywall.)

You’ve probably heard of kleptoplasty, in which some Sacoglossan nudibranch eat algae and digest the algal cells *except for the chloroplasts8. The chloroplasts are kept, for up to a year, in these specialized structures (the nudibranchs look a cool green because they have so many chloroplasts). To test to see if the chloroplasts remained active and the sea slugs were living off of photosynthate, a variety of studies were done, including one where they demonstrated O2 production. This led to speculation that the chloroplasts might also allow the sea slugs to go into anoxic environments, bringing their own O2 generating equipment. I don’t know if the last part was ever demonstrated, though.

Wow! New kingdoms? I’ll have to look up that paper. It’s good to be reminded of how little we know. While I’m into space, we’ve got enough to explore in the sea and other dark places on our own planet.

I’m confused about one thing – why does the presence of eggs in the loriciferans indicate that they live all their lives in anoxic environments? Couldn’t it be possible that they move into oxygenated environments to breed?

I think there still is the possibility that they do this. However, I think the assumption is that if they were leaving to mate and thus were capable of consuming oxygen, we wouldn’t find ANY signs of “pregnancy” whatsoever in the depths. This evidence added to the replacement of mitochondria with these anaerobic hydrosenosomes makes it even more likely that they spend their whole lives there.

In any case, the females are clearly able to develop eggs (or egg-like gametes) in that environment showing that they are there for multiple stages of the lifecycle.

Here’s the paragraph of the paper dealing with reproduction:

“Specimens of the undescribed species of both genera Spinoloricus and Rugiloricus had a large oocyte in their ovary, which showed a nucleus containing a nucleolus (Figure 1d, e). This is the first evidence of Loricifera reproducing in the entire deep Mediterranean basin. Microscopic analyses also revealed the presence of empty exuviae from moulting loriciferans (Figure 1g), suggesting that these metazoans did grow in this system. Moreover, scanning electron microscopy confirmed the perfect integrity of these loriciferans (Figure 2), while all of the other meiofaunal taxa were largely damaged or degraded.”

[…] are the only animals able to make carotene, Hannah’s blogpost over at Culturing Science about the discovery of the first multicellular animals that can live without oxygen and Psi Wavefunction’s essays on neutral evolution. So get out there, and read up on the […]